diff --git a/src/cascadia/TerminalConnection/ConptyConnection.cpp b/src/cascadia/TerminalConnection/ConptyConnection.cpp
index 7bb1b399c7f..cecb5c7d759 100644
--- a/src/cascadia/TerminalConnection/ConptyConnection.cpp
+++ b/src/cascadia/TerminalConnection/ConptyConnection.cpp
@@ -325,7 +325,7 @@ namespace winrt::Microsoft::Terminal::TerminalConnection::implementation
         // handoff from an already-started PTY process.
         if (!_inPipe)
         {
-            DWORD flags = PSEUDOCONSOLE_RESIZE_QUIRK | PSEUDOCONSOLE_WIN32_INPUT_MODE;
+            DWORD flags = PSEUDOCONSOLE_RESIZE_QUIRK;
 
             // If we're using an existing buffer, we want the new connection
             // to reuse the existing cursor. When not setting this flag, the
diff --git a/src/cascadia/UnitTests_TerminalCore/ConptyRoundtripTests.cpp b/src/cascadia/UnitTests_TerminalCore/ConptyRoundtripTests.cpp
index dc66b3a03ed..cd9ac092898 100644
--- a/src/cascadia/UnitTests_TerminalCore/ConptyRoundtripTests.cpp
+++ b/src/cascadia/UnitTests_TerminalCore/ConptyRoundtripTests.cpp
@@ -1200,7 +1200,9 @@ void ConptyRoundtripTests::PassthroughHardReset()
     }
 
     // Write a Hard Reset VT sequence to the host, it should come through to the Terminal
+    // along with a DECSET sequence to re-enable win32 input and focus events.
     expectedOutput.push_back("\033c");
+    expectedOutput.push_back("\033[?9001;1004h");
     hostSm.ProcessString(L"\033c");
 
     const auto termSecondView = term->GetViewport();
diff --git a/src/host/ConsoleArguments.cpp b/src/host/ConsoleArguments.cpp
index 2541cc8ab82..3621bca387f 100644
--- a/src/host/ConsoleArguments.cpp
+++ b/src/host/ConsoleArguments.cpp
@@ -20,7 +20,6 @@ const std::wstring_view ConsoleArguments::WIDTH_ARG = L"--width";
 const std::wstring_view ConsoleArguments::HEIGHT_ARG = L"--height";
 const std::wstring_view ConsoleArguments::INHERIT_CURSOR_ARG = L"--inheritcursor";
 const std::wstring_view ConsoleArguments::RESIZE_QUIRK = L"--resizeQuirk";
-const std::wstring_view ConsoleArguments::WIN32_INPUT_MODE = L"--win32input";
 const std::wstring_view ConsoleArguments::FEATURE_ARG = L"--feature";
 const std::wstring_view ConsoleArguments::FEATURE_PTY_ARG = L"pty";
 const std::wstring_view ConsoleArguments::COM_SERVER_ARG = L"-Embedding";
@@ -515,12 +514,6 @@ void ConsoleArguments::s_ConsumeArg(_Inout_ std::vector<std::wstring>& args, _In
             s_ConsumeArg(args, i);
             hr = S_OK;
         }
-        else if (arg == WIN32_INPUT_MODE)
-        {
-            _win32InputMode = true;
-            s_ConsumeArg(args, i);
-            hr = S_OK;
-        }
         else if (arg == CLIENT_COMMANDLINE_ARG)
         {
             // Everything after this is the explicit commandline
@@ -677,10 +670,6 @@ bool ConsoleArguments::IsResizeQuirkEnabled() const
 {
     return _resizeQuirk;
 }
-bool ConsoleArguments::IsWin32InputModeEnabled() const
-{
-    return _win32InputMode;
-}
 
 #ifdef UNIT_TESTING
 // Method Description:
diff --git a/src/host/ConsoleArguments.hpp b/src/host/ConsoleArguments.hpp
index bb4a95b21e6..8648c92ea66 100644
--- a/src/host/ConsoleArguments.hpp
+++ b/src/host/ConsoleArguments.hpp
@@ -55,7 +55,6 @@ class ConsoleArguments
     short GetHeight() const;
     bool GetInheritCursor() const;
     bool IsResizeQuirkEnabled() const;
-    bool IsWin32InputModeEnabled() const;
 
 #ifdef UNIT_TESTING
     void EnableConptyModeForTests();
@@ -74,7 +73,6 @@ class ConsoleArguments
     static const std::wstring_view HEIGHT_ARG;
     static const std::wstring_view INHERIT_CURSOR_ARG;
     static const std::wstring_view RESIZE_QUIRK;
-    static const std::wstring_view WIN32_INPUT_MODE;
     static const std::wstring_view FEATURE_ARG;
     static const std::wstring_view FEATURE_PTY_ARG;
     static const std::wstring_view COM_SERVER_ARG;
@@ -144,7 +142,6 @@ class ConsoleArguments
     DWORD _signalHandle;
     bool _inheritCursor;
     bool _resizeQuirk{ false };
-    bool _win32InputMode{ false };
 
     [[nodiscard]] HRESULT _GetClientCommandline(_Inout_ std::vector<std::wstring>& args,
                                                 const size_t index,
diff --git a/src/host/VtIo.cpp b/src/host/VtIo.cpp
index b0f4ebad2c3..5d33e607931 100644
--- a/src/host/VtIo.cpp
+++ b/src/host/VtIo.cpp
@@ -71,7 +71,6 @@ VtIo::VtIo() :
 {
     _lookingForCursorPosition = pArgs->GetInheritCursor();
     _resizeQuirk = pArgs->IsResizeQuirkEnabled();
-    _win32InputMode = pArgs->IsWin32InputModeEnabled();
     _passthroughMode = pArgs->IsPassthroughMode();
 
     // If we were already given VT handles, set up the VT IO engine to use those.
@@ -269,10 +268,7 @@ bool VtIo::IsUsingVt() const
     // win32-input-mode from them. This will enable the connected terminal to
     // send us full INPUT_RECORDs as input. If the terminal doesn't understand
     // this sequence, it'll just ignore it.
-    if (_win32InputMode)
-    {
-        LOG_IF_FAILED(_pVtRenderEngine->RequestWin32Input());
-    }
+    LOG_IF_FAILED(_pVtRenderEngine->RequestWin32Input());
 
     // MSFT: 15813316
     // If the terminal application wants us to inherit the cursor position,
diff --git a/src/host/VtIo.hpp b/src/host/VtIo.hpp
index e47d37d9ef6..a15653ad084 100644
--- a/src/host/VtIo.hpp
+++ b/src/host/VtIo.hpp
@@ -67,7 +67,6 @@ namespace Microsoft::Console::VirtualTerminal
         bool _lookingForCursorPosition;
 
         bool _resizeQuirk{ false };
-        bool _win32InputMode{ false };
         bool _passthroughMode{ false };
         bool _closeEventSent{ false };
 
diff --git a/src/host/srvinit.cpp b/src/host/srvinit.cpp
index e1df6552c17..284f4483820 100644
--- a/src/host/srvinit.cpp
+++ b/src/host/srvinit.cpp
@@ -603,11 +603,9 @@ try
     outPipeTheirSide.reset();
     signalPipeTheirSide.reset();
 
-    // GH#13211 - Make sure we request win32input mode and that the terminal
-    // obeys the resizing quirk. Otherwise, defterm connections to the Terminal
-    // are going to have weird resizing, and aren't going to send full fidelity
-    // input messages.
-    const auto commandLine = fmt::format(FMT_COMPILE(L" --headless --resizeQuirk --win32input --signal {:#x}"),
+    // GH#13211 - Make sure the terminal obeys the resizing quirk. Otherwise,
+    // defterm connections to the Terminal are going to have weird resizing.
+    const auto commandLine = fmt::format(FMT_COMPILE(L" --headless --resizeQuirk --signal {:#x}"),
                                          (int64_t)signalPipeOurSide.release());
 
     ConsoleArguments consoleArgs(commandLine, inPipeOurSide.release(), outPipeOurSide.release());
diff --git a/src/inc/conpty-static.h b/src/inc/conpty-static.h
index 89b20468408..4d22048868c 100644
--- a/src/inc/conpty-static.h
+++ b/src/inc/conpty-static.h
@@ -24,7 +24,6 @@
 #endif
 
 #define PSEUDOCONSOLE_RESIZE_QUIRK (2u)
-#define PSEUDOCONSOLE_WIN32_INPUT_MODE (4u)
 #define PSEUDOCONSOLE_PASSTHROUGH_MODE (8u)
 
 CONPTY_EXPORT HRESULT WINAPI ConptyCreatePseudoConsole(COORD size, HANDLE hInput, HANDLE hOutput, DWORD dwFlags, HPCON* phPC);
diff --git a/src/renderer/vt/state.cpp b/src/renderer/vt/state.cpp
index e5ddb08514d..29a8657cd5a 100644
--- a/src/renderer/vt/state.cpp
+++ b/src/renderer/vt/state.cpp
@@ -541,6 +541,9 @@ void VtEngine::SetTerminalCursorTextPosition(const til::point cursor) noexcept
 // - S_OK if we succeeded, else an appropriate HRESULT for failing to allocate or write.
 HRESULT VtEngine::RequestWin32Input() noexcept
 {
+    // It's important that any additional modes set here are also mirrored in
+    // the AdaptDispatch::HardReset method, since that needs to re-enable them
+    // in the connected terminal after passing through an RIS sequence.
     RETURN_IF_FAILED(_RequestWin32Input());
     RETURN_IF_FAILED(_RequestFocusEventMode());
     RETURN_IF_FAILED(_Flush());
diff --git a/src/terminal/adapter/adaptDispatch.cpp b/src/terminal/adapter/adaptDispatch.cpp
index d17d3b740a8..1a0467f7f6f 100644
--- a/src/terminal/adapter/adaptDispatch.cpp
+++ b/src/terminal/adapter/adaptDispatch.cpp
@@ -3055,11 +3055,21 @@ bool AdaptDispatch::HardReset()
         _macroBuffer = nullptr;
     }
 
-    // GH#2715 - If all this succeeded, but we're in a conpty, return `false` to
-    // make the state machine propagate this RIS sequence to the connected
-    // terminal application. We've reset our state, but the connected terminal
-    // might need to do more.
-    return !_api.IsConsolePty();
+    // If we're in a conpty, we need flush this RIS sequence to the connected
+    // terminal application, but we also need to follow that up with a DECSET
+    // sequence to re-enable the modes that we require (namely win32 input mode
+    // and focus event mode). It's important that this is kept in sync with the
+    // VtEngine::RequestWin32Input method which requests the modes on startup.
+    if (_api.IsConsolePty())
+    {
+        auto& stateMachine = _api.GetStateMachine();
+        if (stateMachine.FlushToTerminal())
+        {
+            auto& engine = stateMachine.Engine();
+            engine.ActionPassThroughString(L"\033[?9001;1004h");
+        }
+    }
+    return true;
 }
 
 // Routine Description:
diff --git a/src/winconpty/winconpty.cpp b/src/winconpty/winconpty.cpp
index e964a5691a3..10cfa1fea36 100644
--- a/src/winconpty/winconpty.cpp
+++ b/src/winconpty/winconpty.cpp
@@ -133,19 +133,17 @@ HRESULT _CreatePseudoConsole(const HANDLE hToken,
     RETURN_IF_WIN32_BOOL_FALSE(SetHandleInformation(signalPipeConhostSide.get(), HANDLE_FLAG_INHERIT, HANDLE_FLAG_INHERIT));
 
     // GH4061: Ensure that the path to executable in the format is escaped so C:\Program.exe cannot collide with C:\Program Files
-    auto pwszFormat = L"\"%s\" --headless %s%s%s%s--width %hu --height %hu --signal 0x%x --server 0x%x";
+    auto pwszFormat = L"\"%s\" --headless %s%s%s--width %hu --height %hu --signal 0x%x --server 0x%x";
     // This is plenty of space to hold the formatted string
     wchar_t cmd[MAX_PATH]{};
     const BOOL bInheritCursor = (dwFlags & PSEUDOCONSOLE_INHERIT_CURSOR) == PSEUDOCONSOLE_INHERIT_CURSOR;
     const BOOL bResizeQuirk = (dwFlags & PSEUDOCONSOLE_RESIZE_QUIRK) == PSEUDOCONSOLE_RESIZE_QUIRK;
-    const BOOL bWin32InputMode = (dwFlags & PSEUDOCONSOLE_WIN32_INPUT_MODE) == PSEUDOCONSOLE_WIN32_INPUT_MODE;
     const BOOL bPassthroughMode = (dwFlags & PSEUDOCONSOLE_PASSTHROUGH_MODE) == PSEUDOCONSOLE_PASSTHROUGH_MODE;
     swprintf_s(cmd,
                MAX_PATH,
                pwszFormat,
                _ConsoleHostPath(),
                bInheritCursor ? L"--inheritcursor " : L"",
-               bWin32InputMode ? L"--win32input " : L"",
                bResizeQuirk ? L"--resizeQuirk " : L"",
                bPassthroughMode ? L"--passthrough " : L"",
                size.X,